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Alleviation effects of Bifidobacterium breve on DSS-induced colitis depends on intestinal tract barrier maintenance and gut microbiota modulation

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Abstract

Purpose

The study aimed to investigate the discrepancy and potential mechanisms of different CLA-producing B. breve on dextran sulphate sodium (DSS)-induced colitis.

Methods

Colitis was induced in C57BL/6 J mice using DSS. Disease activity index (DAI), histopathological changes, epithelial barrier integrity and epithelial apoptosis were determined. Gut microbiota were gauged to evaluate the systemic effects of CLA-producing B. breve.

Results

Oral administration of different B. breve showed different effects, in which B. breve M1 and B. breve M2 alleviated the inflammation induced by DSS as well as significantly increased the concentration of mucin2 (MUC2) and goblet cells, but neither B. breve M3 nor B. breve M4 had those protective effects. Meanwhile, B. breve M1 and B. breve M2 treatments significantly up-regulated the tight junction (TJ) proteins and ameliorated the epithelial apoptosis lead by DSS challenge. Moreover, inflammatory cytokines (TNF-α, IL-6) were modulated by B. breve M1 and B. breve M2, neither B. breve M3 nor B. breve M4. Furthermore, B. breve M1 and B. breve M2 reduced the abundance of Bacteroides and increased the abundance of Odoribacter, then rebalanced the damaged gut microbiota. Colonic CLA concentrations in mice fed with B. breve M1, B. breve M2, B. breve M3 and B. breve M4 decreased successively, which showed significant positive correlation with the effectiveness of relieving colitis.

Conclusions

Bifidobacterium breve M1 and B. breve M2 alleviated DSS-induced colitis by producing CLA, inhibiting the inflammatory cytokines, maintaining of the intestinal epithelial barrier and regulating the gut microbiota.

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Abbreviations

IBD:

Inflammatory bowel disease

UC:

Ulcerative colitis

DAI:

Disease activity index

CLA:

Conjugated linoleic acid

H&E:

Haematoxylin and Eosin

MPO:

Myeloperoxidase

COX-2:

Cyclooxygenase 2

iNOS:

Inducible nitric oxide synthase

SOD:

Superoxide dismutase

MDA:

Malonic dialdehyde

CAT:

Catalase

GSH-PX:

Glutathione peroxidase

TJ:

Tight junction

MUC2:

Mucin2

AJ:

Adheres junction

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Acknowledgements

This research was supported by the National Natural Science Foundation of China (Nos. 31801521, 31722041, 31820103010), National First-Class Discipline Program of Food Science and Technology (JUFSTR20180102), the Fundamental Research Funds for the Central Universities (JUSRP52003B), Postgraduate Research & Practice Innovation Program of Jiangsu Province (KYCX19_1829), Wuxi Young Talent Foundation (QNRC075) and the Jiangsu Province “Collaborative Innovation Center for Food Safety and Quality Control”.

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Authors and Affiliations

  1. State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu, China

    Yang Chen, Jianxin Zhao, Hao Zhang, Bo Yang & Wei Chen

  2. School of Food Science and Technology, Jiangnan University, 1800 Lihu Avenue, Wuxi, 214122, Jiangsu, China

    Yang Chen, Jianxin Zhao, Hao Zhang, Bo Yang & Wei Chen

  3. International Joint Research Center for Probiotics and Gut Health, Jiangnan University, Wuxi, Jiangsu, China

    Catherine Stanton, R. Paul Ross & Bo Yang

  4. Teagasc Food Research Centre, Moorepark, Fermoy, Cork, Ireland

    Catherine Stanton

  5. APC Microbiome Ireland, University College Cork, Cork, Ireland

    Catherine Stanton & R. Paul Ross

  6. Department of Gastroenterology, The Affiliated Wuxi Second People’s Hospital of Nanjing Medical University, Wuxi, Jiangsu, China

    Yan Jin

  7. National Engineering Research Center for Functional Food, Jiangnan University, Wuxi, Jiangsu, China

    Hao Zhang & Wei Chen

  8. Wuxi Translational Medicine Research Center, Jiangsu Translational Medicine Research Institute Wuxi Branch, Wuxi, Jiangsu, China

    Hao Zhang

  9. Beijing Innovation Center of Food Nutrition and Human Health, Beijing Technology and Business University (BTBU), Beijing, China

    Wei Chen

Authors
  1. Yang Chen
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  2. Yan Jin
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  3. Catherine Stanton
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  4. R. Paul Ross
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  5. Jianxin Zhao
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  6. Hao Zhang
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  7. Bo Yang
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  8. Wei Chen
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Contributions

YC performed the experiments and analysed the data. BY, YJ, HZ and WC provided intellectual inputs and designed the experiments. JXZ contributed to the data acquisition. RPR and CS critically reviewed the manuscript. YC and BY wrote the manuscript. BY, YJ, RPR and CS revised the manuscript.

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Correspondence to Yan Jin or Bo Yang.

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Chen, Y., Jin, Y., Stanton, C. et al. Alleviation effects of Bifidobacterium breve on DSS-induced colitis depends on intestinal tract barrier maintenance and gut microbiota modulation. Eur J Nutr 60, 369–387 (2021). https://doi.org/10.1007/s00394-020-02252-x

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